Summary The goal of this project is to understand how different brain regions represent one?s current direction and location to support spatial navigation and memory. Recent decades saw the discovery of several spatial representation patterns in the medial temporal lobe and other deep structures, including spatial cells, such as grid and head-direction cells, and signals in oscillatory power of local field potentials, such as the movement-related theta rhythm and a recent theta band signal for goal proximity to boundaries. We recently developed a new method for identifying detailed navigation-related brain activity typically linked to spatial cells in widespread regions based on large-scale neuronal recordings of field potentials rather than single-cell recordings, bridging the gap between the two types of signals. I used this method to identify hexadirectional modulation patterns of the power of human theta-band (5?8 Hz) field potentials, likely generated by the grid cell network (Maidenbaum et al. 2018, PNAS), and have initial findings of several other similar signals. The grid signal in local field potential has proven to be robust - replicated both by us and by two other independent groups. In this proposal, we seek to leverage this our new approach for identifying specific directional spatial representations form LFP to interrogate the human neural representation of direction and location across widespread brain regions using electrocorticographic and depth recordings (ECoG/iEEG) from neurosurgical patients who perform our novel Virtual and Augmented Reality tasks. Our proposal examines the neural representation of directional spatial behavior comprehensively. First, we will characterize the neural correlates of several different directionally tuned spatial representations in the oscillatory power of local field potentials (Aim 1), bridging the gap between single-cell recordings and other imaging modalities, and between the wide array of neural results from animal-models to the literature on human behavior and fMRI representations. We will then test the activity of a battery of local field potential based spatial signals, including our new gridness signal, the signals established by Aim 1 (heading direction, vectors to goals, boundarie and objects) and several other existing signals (e.g. goal location, planned path distance). We will characterize their attributes in different scenarios based on models from the extensive ?animal? literature, and test how they are extended by the differences in perception and higher-cognitive functions of ?humans? in practical navigation and spatial memory behavioral tasks focused on disorientation and remapping of neural representations (Aim 2). Finally, using novel Augmented Reality (AR) paradigms we will test if behavioral results transfer from virtual environments to augmented tasks in the real world, in which the subject?s proprioceptive, vestibular and locomotion systems are active. We will test the stability of our LFP neural signals in directional paradigms in patients using AR tasks that can be performed from the patient's bed (Aim 3). This proposal will improve our understanding of the brain?s spatial system, support navigation and spatial memory in both people who are healthy or those with spatial deficiencies, and more generally aid in understanding the systems underlying episodic memory deficiencies at large.